Antennal uridine diphosphate (UDP)‐glycosyltransferases in a pest insect: diversity and putative function in odorant and xenobiotics clearance

Abstract

Uridine diphosphate UDP-glycosyltransferases (UGTs) are detoxification enzymes widely distributed within living organisms. They are involved in the biotransformation of various lipophilic endogenous compounds and xenobiotics, including odorants. Several UGTs have been reported in the olfactory organs of mammals and involved in olfactory processing and detoxification within the olfactory mucosa but, in insects, this enzyme family is still poorly studied. Despite recent transcriptomic analyses, the diversity of antennal UGTs in insects has not been investigated. To date, only three UGT cDNAs have been shown to be expressed in insect olfactory organs. In the present study, we report the identification of eleven putative UGTs expressed in the antennae of the model pest insect Spodoptera littoralis. Phylogenetic analysis revealed that these UGTs belong to five different families, highlighting their structural diversity. In addition, two genes, UGT40R3 and UGT46A6, were either specifically expressed or overexpressed in the antennae, suggesting specific roles in this sensory organ. Exposure of male moths to the sex pheromone and to a plant odorant differentially downregulated the transcription levels of these two genes, revealing for the first time the regulation of insect UGTs by odorant exposure. Moreover, the specific antennal gene UGT46A6 was upregulated by insecticide topical application on antennae, suggesting its role in the protection of the olfactory organ towards xenobiotics. This work highlights the structural and functional diversity of UGTs within this highly specialized tissue.

Glutathione-S-Transferases in the Olfactory Organ of the Noctuid Moth Spodoptera littoralis, Diversity and Conservation of Chemosensory Clades

“…In the cotton leafworm S. littoralis , an unsuspected number of CCEs, UGTs, and CYPs had been previously described in antenna (Durand et al, 2010b; Pottier et al, 2012; Bozzolan et al, 2014), leading to the hypothesis that antennal enzymes could participate in signal inactivation and odorant clearance as Odorant-Degrading Enzymes, but also in detoxification processes. Indeed, various airborne compounds, such as toxic allelochemicals emitted by plants or anthropic xenobiotics could enter the olfactory sensilla and reach the olfactory receptor neurons (ORNs) and potentially harm them (Siaussat et al, 2014).…”

“…In this pest species, transcriptomic approaches (Legeai et al, 2011; Jacquin-Joly et al, 2012) have already led to the identification of various olfactory gene repertoires, such as Odorant Receptors and Odorant-Binding Proteins, but also of several phase I and II enzymes, such as CCEs (Durand et al, 2010b), CYPs (Pottier et al, 2012), or UGTs (Bozzolan et al, 2014). Here, using more recent and complete transcriptomic data (Poivet et al, 2013), we identified 33 putative GSTs expressed in the antennae of this species.…”

Venom allergen 5is Associated With Deltamethrin Resistance inCulex pipiens pallens(Diptera: Culicidae)

“…We speculate that venom allergen 5 is important for cell growth and development. This gene may be a multifunctional protein, performing different functions at different stages, as do the insect UDP-glycosyltransferases that play important roles in detoxication of xenobiotics, cuticle formation, pigmentation, and olfaction (Huang et al 2008, Bozzolan et al 2014. The specific biological function of venom allergen 5 in Cx.…”

“…In addition, insecticides induce physiological changes in mosquitoes such as a thickening of the epidermis, which subsequently lowers their permeability to insecticides (Wood et al 2010). Studies investigating the mechanisms of pyrethroid resistance have identified other resistance-related genes, such as UDP-glycosyltransferases , Bozzolan et al 2014) and serine proteases (Reid et al 2012, Strachecka et al 2013.…”

Comparative transcriptome analyses of deltamethrin-susceptible and -resistant Culex pipiens pallens by RNA-seq

“…Moreover, pyrethroid insecticides cause the physiological changes of mosquitoes, such as the epidermal thickening, which subsequently reduces the absorption or penetration of insecticides (Wood et al 2010). Other pyrethroid resistance-related genes have also been identified, such as UDP-glucuronosyltransferases (Bozzolan et al 2014) and serine proteases (Reid et al 2012). However, the pyrethroid resistance results from polygenic inheritance (Ffrench-Constant et al 2004).…”